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Revealing the Immune Perturbation of Black Phosphorus Nanomaterials to Macrophages by Understanding the Protein Corona ARTICLE DOI: 10.1038/s41467-018-04873-7 OPEN Revealing the immune perturbation of black phosphorus nanomaterials to macrophages by understanding the protein corona Jianbin Mo 1,2, Qingyun Xie3, Wei Wei 1,2 & Jing Zhao 1 The increasing number of biological applications for black phosphorus (BP) nanomaterials has precipitated considerable concern about their interactions with physiological systems. 1234567890():,; Here we demonstrate the adsorption of plasma protein onto BP nanomaterials and the subsequent immune perturbation effect on macrophages. Using liquid chromatography tandem mass spectrometry, 75.8% of the proteins bound to BP quantum dots were immune relevant proteins, while that percentage for BP nanosheet–corona complexes is 69.9%. In particular, the protein corona dramatically reshapes BP nanomaterial–corona complexes, influenced cellular uptake, activated the NF-κB pathway and even increased cytokine secretion by 2–4-fold. BP nanomaterials induce immunotoxicity and immune per- turbation in macrophages in the presence of a plasma corona. These findings offer important insights into the development of safe and effective BP nanomaterial-based therapies. 1 State Key Laboratory of Coordination Chemistry, Institute of Chemistry and BioMedical Sciences, School of Chemistry and Chemical Engineering Nanjing University, Nanjing 210093, China. 2 State Key Laboratory of Pharmaceutical Biotechnology, School of Life Sciences, Nanjing University, Nanjing 210093, China. 3 Department of Orthopedics, Chengdu Military General Hospital, Chengdu 610083, China. These authors contributed equally: Jianbin Mo, Qingyun Xie. Correspondence and requests for materials should be addressed to W.W. (email: [email protected]) or to J.Z. (email: [email protected]) NATURE COMMUNICATIONS | (2018) 9:2480 | DOI: 10.1038/s41467-018-04873-7 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-04873-7 lack phosphorus (BP) crystals have existed for a long time, found to be free-standing with a lateral size of approximately 300 Bbut we have only recently begun to realize their true nm, and BPQDs were found to be approximately 5 nm in size potential from the perspective of two-dimensional (2D) (Fig. 2a, b). According to a statistical TEM analysis of 100 BPQDs nanomaterials1. BP thin film material has been produced from (Fig. 2b), the average lateral size of a BPQD is 5.7 ± 1.0 nm (values bulk BP crystals through the exfoliation method, and this material are expressed as the means ± SDs of triplicates). The BPQDs and exhibits unique qualities such as thickness-dependent band gap BPNSs were also characterized by X-ray photoelectron spectro- and high carrier mobility2,3. While many breakthroughs have scopy (XPS) and Raman spectroscopy. As shown in Fig. 2c, the been made regarding nanoelectronic applications for BP nano- similar prominent peaks from BPQDs and BPNSs can be 4 1 −1 materials , studies on extensive applications in biomedicine and attributed to one out-of-plane phonon mode (A g) at 356.8 cm biotechnology have become more common. Several groups have as well as two in-plane modes, B and A2, at 432.3 and 459.6 cm − 2g g reported that BP nanomaterials could serve as high-efficiency 1, respectively. Furthermore, similar survey XPS spectra for photosensitizers for photodynamic therapy and drug delivery BPQDs and BPNSs document the similar surface chemistry of – systems with ultra-high loading capacity5 8. Recently, potential these two BP nanomaterials (Fig. 2d). Taken together, the data inflammatory effects of BP nanomaterials have been reported9. indicate that size is the key difference between BPQDs and However, understanding of their actual biological effects on BPNSs. physiological systems is limited. Numerous studies have shown visual images of the corona on It has now been established that the surfaces of nanomaterials nanospheres or nanorods, but nanosheet coronas have rarely are immediately covered by a plasma protein corona when they been reported. Therefore, to provide additional qualitative come into contact with blood10,afinding that has led to the support for the stability of the isolated BP–corona complexes, redefinition of the biological properties of nanoparticles (NPs) we present TEM images of BPQDs and BPNSs with protein 11,12. Chen et al. elegantly demonstrated binding of the bovine corona (Fig. 2e, f). In BPNS–protein corona complexes, the serum albumin (BSA) protein corona to Au nanorods and surfaces of the BPNSs were strikingly different from their native revealed reduced damage to cell membranes13. Dawson et al. have forms, and the zeta-potential values of BPNSs decreased from made pivotal progress on understanding the role of the protein −18.1 to −8.4 mV (Fig. 2i), suggesting adsorption of plasma corona in the loss of targeting capabilities of NPs14. proteins onto the BPNSs. The size of BPNS–corona nanomater- The implications of nanomaterial–corona complexes are far ials was also investigated by dynamic light scattering (DLS) reaching, suggesting that the biological impacts of nanomaterials analysis (Fig. 2g and Supplementary Table 1). The results showed on a physiological system cannot simply be linked to the nature of that the average size of BPNSs changed from 338.4 ± 2.3 to 365.3 the nanomaterial alone. Therefore, for continued development of ± 5.9 nm. Unexpectedly, after the protein corona was formed on BP nanomaterials in biomedicine, studies on interactions between the surface of BPQDs, BPQDs were redefined from ultra-small nanomaterials and plasma proteins and the influence on immune nanosheets to spherical BPQD–corona complex NPs, and the NPs cells are urgent. Here we study the protein corona formed by appeared to be bulky particles with a diameter of approximately exposing different sizes of BP nanomaterials to plasma proteins 371.9 ± 9.1 nm (Fig. 2b, f). The zeta-potential values of BPQDs and demonstrated their immune perturbation effect on macro- decreased from −20.6 to −6.4 mV, and the “wet” diameter phage (Fig. 1). Our results also highlight the importance of increased from 5.6 ± 1.4 to 362.5 ± 5.6 nm (Fig. 2h, i and nanomaterial size on protein corona formation and could further Supplementary Table 1). Energy dispersive X-ray spectroscopic redefine BP nanomaterials and the biological response to BP (EDX) analysis further verified that BPQD was in the corona nanomaterials. complex (Supplementary Figure 1). Results Identification of the plasma corona. According to the literature, Characterization of nanomaterials. First, BP nanosheets the formation of plasma proteins on the surfaces of nanomaterials (BPNSs) and BP quantum dots (BPQDs) were obtained according can occur almost instantly after nanomaterials enter the blood15. to reported methods5,7 and analysed by transmission electron The zeta-potential values for BP nanomaterials showed that the microscopy (TEM). From the TEM image results, BPNSs were high initial values (−20.6 mV for BPQDs and −18.1 mV for Vessel Cytokines BP nanomaterial NF-κB ROS BP–corona Macrophage complex Fig. 1 Summary diagram of immune perturbation of BP–corona complexes. Formation of BP nanomaterial–corona complexes in blood and their immunoregulation on macrophages 2 NATURE COMMUNICATIONS | (2018) 9:2480 | DOI: 10.1038/s41467-018-04873-7 | www.nature.com/naturecommunications NATURE COMMUNICATIONS | DOI: 10.1038/s41467-018-04873-7 ARTICLE ace 2 BPNSs 1 A g 1000 A g BPQDs 800 B2g 600 400 Raman intensity 200 0 350400 450 500 550 Raman shift (cm–1) bd f 25 N=100 O 1s BPNSs 20 N=100 20 5.7±1.0 nm 371.9±9.1 nm BPQDs 15 15 10 10 Number of particles 5 5 P 2s Number of particles 0 0 3456789 P 2p 100 200 300 400 500 600 700 Diameter (nm) Diameter (nm) Counts (s) 800 600 400 200 0 Binding energy (eV) BP gh i BP –corona 0 120 BPNSs 120 BPQDs BPNSs–corona complexes BPQDs–corona complexes 100 100 –5 80 80 –10 60 60 Number Number 40 40 –15 20 20 Zeta potential (mV) –20 BPQDs 0 0 BPNSs 120 240 360 480 600 4 5 6 7 300 360 420 Size (nm) Size (nm) Fig. 2 Image of BP nanomaterials and corona complexes. a TEM image of a BPNS. Scale bar: 200 nm. b TEM image of BPQDs. Inset: statistical analysis of the size of 100 BPQDs determined by TEM. Scale bar: 200 nm. c Raman spectra of BPQDs and BPNSs. d XPS spectra of BPQDs and BPNSs. e TEM image of a BPNS–corona complex. Scale bar: 50 nm. f TEM image of BPQD–corona complex. Inset: statistical analysis of the size of 100 BPQD–corona complexes determined by TEM. Scale bar: 500 nm. g Dynamic light scattering (DLS) analysis of BPNSs and BPNS–corona complexes. h DLS analysis of BPQDs and BPQD–corona complexes. i Zeta potential of BP nanomaterials and BP–corona complexes. Values are expressed as the means ± SDs of triplicates BPNSs) were reduced after entry (to −7.3 mV for BPQDs and the intensity of a fixed band, the 40 KD marker band in the first −13.7 mV for BPNSs in 0.5 h), suggesting that the proteins were lane) of several bands marked with an asterisk from the gels in adsorbed onto BP nanomaterials in a short time (Supplementary Fig. 3a, b. As shown in Fig. 3d, 55 and 60 KD proteins were main Figure 2). Then BP nanomaterials, including BPNSs and BPQDs, components in corona at low plasma concentration, while other were exposed to blood plasma of different concentrations for 4 h. proteins (i.e., 35, 70 and 180 KD protein) dominated the corona Plasma proteins in corona were then separated by sodium composition at high plasma concentration. These data suggested dodecyl sulphate-polyacrylamide gel electrophoresis (SDS- that the size of BP nanomaterials played a key role in determining PAGE). As Fig. 3a shows, with an increasing plasma concentra- the BP–corona complexes.
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